Morphological and anatomical characteristics of ...

Acta Zoologica Lituanica

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MORPHOLOGICAL AND ANATOMICAL CHARACTERISTICS OF OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA: SUCCINEIDAE) Ingrida Šatkauskienė To cite this article: Ingrida Šatkauskienė (2007) MORPHOLOGICAL AND ANATOMICAL CHARACTERISTICS OF OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA: SUCCINEIDAE), Acta Zoologica Lituanica, 17:4, 333-340, DOI: 10.1080/13921657.2007.10512851 To link to this article: http://dx.doi.org/10.1080/13921657.2007.10512851

Published online: 23 Jul 2012.

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Acta Zoologica Lituanica, 2007, Volumen 17, Numerus 4 ISSN 1392-1657

MORPHOLOGICAL AND ANATOMICAL CHARACTERISTICS OF OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA: SUCCINEIDAE) Ingrida ÐATKAUSKIENË

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Department of Biology, Vytautas Magnus University, Vileikos 8, LT-44404 Kaunas, Lithuania. E-mail: [email protected] Abstract. Identification of Oxyloma sarsi is confused by the similarity of its shell to those of other succineid species. In this paper, morphological criteria (shape, colour and size of the shells (measurements), the reproduction system and the structure of the radula) for identification of O. sarsi are reconsidered. New data dealing with morphological identification of O. sarsi are presented: body pigmentation, the shape and size of the ‘jaw’, and the parameters of the reproductive system (length of the vagina and oviductus). Key words: Succineidae, Oxyloma, reproduction system, identification

INTRODUCTION The distribution of molluscs of the family Succineidae is worldwide (Kerney & Cameron 1979; Pfleger 1999). Four species of the family Succineidae are found in Europe and Lithuania: Succinea putris (Linnaeus, 1758), Succinella oblonga (Draparnaud, 1801), Oxyloma sarsi (Esmark, 1886) and Oxyloma elegans (Risso, 1826) (Gurskas 1997; Kerney 1999; Pfleger 1999; Ðivickis 1960). There are only few groups in the worldwide terrestrial malacofauna that have so pronounced outward appearance as the representatives of the family Succineidae. Because of the specific appearance of the shell, Succineidae are easily distinguishable from other families. However, within the family, different Succineidae species usually cannot be distinguished by conchological characters and therefore can be identified only by their anatomy, which includes not only anatomical analysis of the genital structure, but also the arrangement and proportion of the organs (Gusarov 1999; Kerney 1999; Patterson 1971; Rigby 1965). In addition, more precise identification requires analysis of an animal’s pigmentation, colour and shape of the shell, degree of shell calcification, size and habits of an individual (Hoagland & Davis 1987; Patterson 1971; Spamer & Bogan 1998). There are many publications that analysed Succineidae in North America (Hoagland & Davis 1987; Patterson 1971; Spamer & Bogan 1998; Stevens et al. 1998). However, biology and systematics of the genera Oxyloma (Wester-

lund, 1885) and Succinea (Draparnaud, 1801) are not extensively investigated in Europe, including Lithuania. In the guide to Lithuanian molluscs, Ðivickis (1960) described various Succineidae species basically according to their conchological characteristics and therefore according to this guide precise identification of the species is impossible. In another guide Gurskas (1997) presented morphological characteristics of the species Succineidae and the schemes of the reproduction system of three Succineidae species: S. putris, O. elegans and O. sarsi according to Kerney et al. (1983), Shileiko and Likharev (1986) and Grossu (1988). However, some schemes are ambiguous, which again in some cases does not allow precise identification of the species. The entire genus Oxyloma requires extensive review and illustration. The species O. sarsi is treated as endangered by Kerney (1999). Kerney (1999) mentioned that ‘O. sarsi now is found only in a few places in the Lea valley in Herts and Essex, the lower Waveney valley and in the East Anglian Broadland. Surviving populations are at constant risk that originates from pollution. Vulnerable. N. European: known from the scattered areas between the Alps and northern Scandinavia’. Meanwhile, the distribution and situation of this species in Lithuania are unknown due to its difficult identification and misidentification with the other species of Succineidae. The aim of this paper is to present morphological-anatomical characteristics of one species of the genus Oxyloma (family Succineidae), Oxyloma sarsi.

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MATERIAL AND METHODS Adult individuals (N = 118) of Oxyloma sarsi (Esmark, 1886) were collected in May–July 2005 from two populations in the Kaunas district: Domeikava (population I) and Vaiðvydava (population II) villages. Specimens from population I were taken from the coast of the Neris River at the very proximity of water having a sandy substrate. Composition of vegetation in the biotope was: Polygonatum sp. – Artemisia spp. – Equisetum spp. – Poa spp. – Salex spp. Population II was collected in a wet grassland, near a mixed deciduous forest. Composition of the biotope was: Carex spp. – Polygonatum spp. – Taraxacum officinale L. – Poa spp. Collected molluscs were frozen at -20°C. In these conditions, molluscs may be kept for long periods and used when needed for anatomical or DNA analysis. The main part of the collected individuals (N = 118) was used for morphological-anatomical analysis. Another part (N = 18) was used for culture in the laboratory, where the ecology and biology (reproduction, development, life time) of the specimens were observed. The sample of the foot of some individuals (N = 10) was removed and preserved in 70% ethanol for DNA analysis. Before anatomical analysis, the shells of the molluscs were removed, cleaned and kept in dry vials. The genital systems, jaws, radula and the fragments of the mantle were prepared from the molluscs and stored in 70% ethanol. In order to analyse the penial appendix and epiphallus, the penial sheath was opened and pinned up to reveal the details of their structure. Photographs of the shells, molluscs and reproduction systems were

Figure 1. Alive O. sarsi (Esmark, 1886) molluscs at copulation.

Ðatkauskienë I.

taken by using a digital camera Nikon Cool Pix 5200. Parts of the genital systems and jaws were measured and photographed through a stereoscopic microscope MOTIC BA4000 with a digital camera Canon D350. The software used was MOTIC IMAGES Plus 2.0. The radula and the fragments of the mantle were photographed by using a microscope PZO (Poland) at magnification 140× and 280×. Shell length and width, and aperture length and width were measured. Data were represented as a mean ± standard deviation (sample size, minimum and maximum values). The correlation coefficient between shell parameters (shell length and width, and aperture length and width) were calculated with Analysis ToolPak (MS Excel). Preliminary identification of species was performed by using the guides to molluscs by Pfleger (1999), and Kerney and Cameron (1979).

RESULTS Morphological characteristics The shell of alive O. sarsi mollusc is dark or black (Fig. 1). According to Ðivickis (1960), some variations in colour and form of this species can be observed. During this study, however, none of these variations did occur. The empty shell of O. sarsi is thin, amber-coloured (there is a little variation in colouring), translucent and consists of 3 whorls (Fig. 2). The first whorl is large and clearly separated from the remaining whorls. The sutures of the whorls are clear and profound. The surface of the shell is glossy, transversely striped. The edge of the shell aperture is thin, with slight incurvature and lips. The average height and width of the shells of the specimens from the two populations were 9.03 ± 1.48 (N = 118; Min – 7; Max – 14) and 4.25 ± 0.57 mm (N = 118; Min – 3; Max – 6), respectively. Height and width of the aperture of the shells were 6.28 ± 0.94 (N = 61; Min – 4.5; Max – 8.9) and 3.71 ± 0.72 mm (N = 61; Min – 2.9; Max – 5.9), respectively. In order to verify whether there is correlation between size parameters of the shell, the correlation coefficient was calculated between shell length and width, and aperture height and width. The correlation coefficient, which varied between 0.85 and 0.92, indicated strong correlation between these parameters (Table 1). The sole of O. sarsi is pale, almost transparent. Sides of the body are slightly pigmented, whereas the top of the head is usually darkly pigmented (Fig. 1). The observed pigmentation of the mantle through the microscope showed that the pigmented cells are stellular, separate and have no clear interdependence (Fig. 3).

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Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)

Figure 3. Pigmentation of the pallium of O. sarsi (×140).

Figure 2. The shell of S. putris (Linnaeus, 1758) (A and B) and O. sarsi (Esmark, 1886) (C and D).

Pigmentation of all the investigated individuals of O. sarsi was similar and quite consistent. Characteristics of the radula and jaw The radula of O. sarsi is of an extended rhombus shape. Each tooth of the radula consists of a basal plate, lying on the basal lamina, and of a cutting plate, directed backwards, used for food scraping (Jackiewicz 1998). The radular teeth are arranged in parallel longitudinal rows and distinguished by a different structure in the middle and in the lateral sides of the radula. Teeth in the radula are aligned in parallel rows and are distin-

guished by a different structure in the middle and at the edges of the radula. The teeth in the middle of the radula are large, with a splay cusp of the cutting plate (Fig. 4A). The basal plate consists of a large rounded cusp located in the centre and of smaller irregular cusps lying laterally to the central cusp. The lateral teeth are with a rectangular cutting plate (Fig. 4B). The neighbouring small teeth have sharp cusps and cover the basal plate. The number of these teeth can vary from 2 to 5, but the usual number is 5. The jaw of molluscs is built of conchiolin, produced by the epithelial cells of the oral cavity. The jaw is used first and foremost for cutting off larger fragments of food (Jackiewicz 1998). The basal plate of the jaw of O. sarsi is quadrate, thin, light yellow in colour (Fig. 9B). The cutting plate of the jaw is thick, dark brownish, with rounded broad tips. The width of the cutting plate between the tips was: 0.98 ± 0.095 mm (N = 14; Min – 0.85; Max – 1.05). The height of the jaw from the basal to the cutting plate was 0.99 ± 0.065 mm (N = 14; Min – 0.97; Max – 1.05). Characteristics of the reproduction system The uterus (uterus) of O. sarsi is large, having a distinct shape. A thin albumin gland (glandula albuminalis) is separated from the uterus. The vagina (vagina) is thick, long and forms a bend. The oviduct (oviductus) is short, rapidly descending to the uterus. The average

Table 1. The correlation coefficient between shell parameters of Oxyloma sarsi.

Shell length Shell width Aperture height Aperture width

Shell length 1 0.870945 0.881997 0.864413

Shell width

Aperture height

Aperture width

1 0.884864 0.855932

1 0.914969

1

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A

B

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A

B

C

Figure 4. The radula of O. sarsi (K – cutting plate of teeth; Bz – basal plate of teeth): A – medial teeth (×280); B – lateral teeth (×140).

Figure 5. The interior structure of the penis of O. sarsi.

Figure 6. The reproduction system of O. sarsi (A), scheme of the reproduction system (B) and the prepared penial appendix (C): PP – penis; PM – penial sheath; M – vagina; S – vas deferens; SP – spermatheca; SPs – stalk of spermatheca; K – oviductus; P – prostata; G – uterus; A – penial appendix.

length of the vagina is 4.04 mm ± 1.02 (N = 19; Min – 2.63 mm; Max – 5.86 mm). The average length of the oviduct is 2.21 mm ± 0.63 (N = 19; Min – 1.1; Max –

4 mm). The prostate (prostata) is large and elongated. The penis (penis) is mace-shaped, covered by a weakly pigmented penial sheath (Fig. 6A, B). A distinct penial

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Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)

appendix is observed after the removal of the penial sheath (Fig. 6C). The spermatheca is frequently large and spherical in shape. The stalk of the spermatheca is short (Fig. 6A, B). The interior structure of the penis consists of the disorderly, reticulate spread of membrane strands (Fig. 5).

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D ISCUSSION Size, shape and colour of the shell of molluscs, including those involved in this study, can be used as simple and reliable indicators for preliminary identification the genus Oxyloma in field conditions. The molluscs of Oxyloma are small, dark, with an elongated shell and differ considerably from S. putris specimens, which are longer and wider. The average length and width of the shells of O. sarsi and S. putris collected from various populations were 9.03 ± 1.48 (N = 118; Min – 7; Max – 14) and 4.25 ± 0.57 mm (N = 118; Min – 3; Max – 6), and 17.47 mm ± 0.23 mm (N = 74; Min – 12 mm; Max – 22.9 mm) and 8.23 mm ± 0.13 mm (N = 74; Min – 5.5 mm; Max – 10.9 mm), respectively. Statistical analysis showed that these parameters were significantly different between these species (p < 0.0001). The same p value was obtained when comparing height and width of the aperture in both species. Certainly, size indicators cannot be applied to distinguish between juveniles of Oxyloma and S. putris, especially in mixed populations. The size of the collected individuals of O. sarsi are in a relatively good agreement with the measurements of O. sarsi presented by Gusarov (1999), where the average height and width of the shells were 10.2–11.5 and 4.8–6.5 mm, respectively (Table 2). The same agreement is observed when comparing the measurements presented by Ðivickis (1960) (Table 2). Meanwhile, the height of the shell of O. sarsi indicated by Gurskas (1997) is considerably larger than in this study and that reported by other authors (Table 2). One of the reasons for such discrepancy could originate from

misidentification and confusion of O. sarsi with S. putris. As seen from Table 2, many authors (Gurskas 1997; Gusarov 1999; Kerney 1999) indicate only the height and width of the shells, however for precise identification of species the parameters of the aperture are also required. The proportion of the parameters of the shell and aperture reflects a real form of O. sarsi. Table 2 shows that shell parameters of O. sarsi obtained in this study are lower in comparison to those of other authors. This discrepancy is not clear and remains to be explained. Pigmentation of Oxyloma by some features (shape of the pigmented cells and type of connections) (Fig. 3) differed from that of the similar species S. putris, of which the pigmented cells are stellular, distributed irregularly and are interconnected by thin, pigmented strips (Fig. 7). Nevertheless, the pigmentation of the mantle should not be used as a single criterion for species identification. Jackiewicz (1993) reported that colour patterns on the mantle show great diversity, being similar in some species only. Forsyth (2005) mentioned that Succinea strigata could be distinguished from the other species of the family by its shell, jaw and external pigmentation.

Figure 7. Pigmentation of the pallium of S. putris (×280).

Table 2. Comparison of size parameters (in mm) of O. sarsi indicated by various authors.

Average shell parameters Shell height Shell width Aperture height Aperture width * – not indicated

Ðivickis (1960) 10.6 05.3 08.1 04.1

Gurskas (1997) 20.0 05.5 * *

Gusarov (1999) 10.2–11.5 4.8–6.5 * *

Kerney (1999) 12–15 * * *

Present study (2007) 9.03 ± 1.48 4.25 ± 0.57 6.28 ± 0.94 3.71 ± 0.72

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Preliminary analysis of the radula structure led us to propose that the radula can be used as a suitable criterion for identification of the genus Oxyloma and its separation from the species S. putris (Fig. 8). Nevertheless, the differences of the radula structure in O. sarsi and O. elegans are not considerable, which shows that it should not be used as a sole criterion for separation of these two species (unpublished data). The jaw of O. sarsi (Fig. 9B) could be used as one of the criterion to identify this species, because a single rounded and weakly pronounced tooth in the middle of the cutting plate is a specific feature of O. sarsi. The width and height of the jaw of O. sarsi are signifi-

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cantly different (p < 0.0001) from jaw parameters in S. putris (width of the cutting plate between the tips was: 1.5 mm ± 0.2 mm (N = 14; Max – 2.1 mm; Min – 1.2 mm); height of the jaw from the basal to the cutting plate was: 1.2 mm ± 0.1 mm (N = 14; Max – 1.6 mm; Min – 0.9 mm) (Fig. 9). The reproduction system of the investigated specimens of O. sarsi (Fig. 6) showed small variability. Some variations were observed in the shape of the appendix and the length of the stalk of the spermatheca. Despite these small variations, the reproduction system still can A

A

B B

Figure 8. The radula (lateral teeth) of S. putris (×140) (A) and the radula (lateral teeth) of O. sarsi (×140) (B).

Figure 9. The jaw of S. putris (×32) (A) and the jaw of O. sarsi (×32) (B): K – cutting plate; Bz – basal plate.

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Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)

be used as a quite reliable criterion for identification of this species. The salient feature of the reproduction system is the difference between the length of the vagina and oviductus. The average length of the vagina is 4.04 mm ± 1.02 (N = 19; Min – 2.63 mm; Max – 5.86 mm) and that of the oviductus is 2.21 mm ± 0.63 (N = 19; Min – 1.1; Max – 4 mm). Meanwhile, the proportion of the vagina and oviductus of S. putris is converse (Fig. 10). The vagina is shorter: 3.37 mm ± 0.93 mm (N = 23; Max – 4.77 mm; Min – 1.27 mm) and the oviductus is longer: 6.97 mm ± 1.51 mm (N = 23; Max – 9.46 mm; Min – 4.03 mm). Statistical analysis showed that the length of the vagina and oviduct in O. sarsi and S. putris was significantly different (p < 0.0001). Another important feature of the reproduction system of O. sarsi is a distinct penial appendix that is observed after the removal of the penial sheath (Fig. 6C). The penis of O. sarsi is mace-shaped, covered by a weakly pigmented penial sheath, whereas that of S. putris is oblong and waisted (Figs 6, 10). In conclusion, the study shows that the first and preliminary criterion for identification of Oxyloma sarsi (Esmark, 1886) in field conditions could be the parameters of the shell (9.03 × 4.25 mm) and aperture (6.28 × 3.71 mm), the elongated shape of the shell (determined by the proportions of the shell and apertures) and a dark, almost black colour of alive molluscs. The jaw with a single weakly developed tooth in the middle of the cutting plate could be used as the second criterion. For more accurate identification, both criteria must be complemented by extensive analysis of the reproductive system. The distinct features of

Figure 10. The reproduction system of S. putris (modified after Kerney & Cameron 1979): PP – penis; M – vagina; S – vas deferens; SP – spermatheca; SPs – stalk of spermatheca; K – oviductus.

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the reproductive system of O. sarsi are the appendix of the penis (feature of the genus) and the disproportion between the length of the vagina and oviductus (feature of the species).

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Collected works of Zoological Museum of Moscow State University: 7. [Øèëåéêî, À. À., Ëèõàðåâ È. Ì. 1986. Íàçåìíûå ìîëëþñêè ñåìåéñòâà ÿíòàðîê ôàóíû ÑÑÑÐ. Ñáîðíèê Òðóäîâ Çîîìóçåÿ ÌÃÓ: 7.] Solem, A. 1976. Status of Succinea ovalis chittenangoensis Pilsbry, 1908. Nautilus 90 (3): 107–114. Spamer, E. E. and Bogan, A. E. 1998. Contrasting objectives in environmental mediation, reconnaissance biology, and endangered species protection – a case study in the kanab ambersnail, Oxyloma Haydeni Kanabensis Pilsbry 1948 (Gastropoda: Stylommatophora: Succineidae). Walkerana 9 (22): 177–215. Stevens, L. E., Keim, P., Miller, M. and Wu, S. K. 1998– 1999. Succineid landsnail collection data in the United States and Canada. Oxyloma taxonomy Draft Final Report: 10–21. Ðatkauskienë, I. 2005. Characteristic of lifespan and reproduction period of Succinea putris (L.) (Gastropoda: Styllomatophora). Ecology 3: 28–33. Ðivickis, P. 1960. Lithuanian molluscs and their identification. Vilnius: State Publishing House of Political and Scientific Literature.

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Ðatkauskienë I.

MORFOLOGINË-ANATOMINË OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA: SUCCINEIDAE) CHARAKTERISTIKA I. Ðatkauskienë

SANTRAUKA Succineidae ðeimos rûðies Oxyloma sarsi identifikacija yra sudëtinga dël jos panaðumo su kitomis ðios ðeimos rûðimis. Dël ðios prieþasties O. sarsi paplitimo ir gausumo Lietuvoje duomenys gali bûti netikslûs, todël yra bûtina iðryðkinti morfologinius-anatominius kriterijus, kuriais remiantis bûtø galima nustatyti ðià rûðá. Straipsnyje pateikiami O. sarsi kriaukliø matavimo parametrai, radulës ir lytinës sistemos charakteristika. Pirmà kartà pateikiami lytinës sistemos (kiauðintakio, makðties) struktûrø matavimai, „þandikauliø“ ir kûno pigmentacijos charakteristika. Received: 14 November 2006 Accepted: 6 November 2007